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Strong increase of durum wheat iron and zinc content by field-inoculation with arbuscular mycorrhizal fungi at different soil nitrogen availabilities

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Abstract

Background and aims

Since actual production of wheat often leads to human Fe and Zn deficiency, a better understanding of the potential of arbuscular mycorrhizal fungal (AMF) inoculation for micro-nutrient uptake of durum wheat is needed.

Methods

Effects of AMF field inoculation and N availability were evaluated on an old and a modern durum wheat variety

Results

Following AMF inoculation, the modern variety showed a higher increase of the early root colonization respect to the old one, whereas at maturity root colonization was decreased by N fertilization. In the old variety grain N concentration was increased by inoculation when plants were not fertilized and at the 40–0-40 N, whereas in the modern variety inoculation did not change N concentration. By contrast, in AMF inoculated plots the modern variety showed a higher increase of Fe and Zn in grain compared to the old variety. Accordingly, at harvest, the modern variety showed an higher increase of a molecular operational taxonomic unit affiliated to Rhizophagus compared to the old variety.

Conclusion

The inoculated isolate is a good durum wheat colonizer and the modern variety showed higher responsiveness to inoculation in terms of N, Fe and Zn grain concentration respect to the old one.

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References

  • Abbate PE, Pontaroli AC, Lázaro L, Gutheim F (2013) A method of screening for spike fertility in wheat. J Agric Sci 151:322–330

    Article  Google Scholar 

  • Albizua A, Williams A, Hedlund K, Pascual U (2015) Crop rotations including ley and manure can promote ecosystem services in conventional farming systems. Appl Soil Ecol 95:54–61

    Article  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

  • Al-Karaki GN, Al-Raddad A (1997) Effects of arbuscular mycorrhizal fungi and drought stress on growth and nutrient uptake of two wheat genotypes differing in drought resistance. Mycorrhiza 7:83–88

    Article  CAS  Google Scholar 

  • Álvaro F, Royo C, García del Moral LF, Villegas D (2008) Grain Filling and Dry Matter Translocation Responses to Source? Sink Modifications in a Historical Series of Durum Wheat. Crop Sci 48:1523

  • Arduini I, Masoni A, Mariotti M, Pampana S, Ercoli L (2014) Cadmium uptake and translocation in durum wheat varieties differing in grain-Cd accumulation. Plant Soil Environ 60:43–49

  • Augé RM (2001) Water relations, drought and VA mycorrhizal symbiosis. Mycorrhiza 11:3–42

    Article  Google Scholar 

  • Babana AH, Antoun H (2006) Effect of Tilemsi phosphate rock-solubilizing microorganisms on phosphorus uptake and yield of field-grown wheat (Triticum aestivum L.) in Mali. Plant Soil 287:51–58

    Article  CAS  Google Scholar 

  • Bago B, Pfeffer PE, Shachar-Hill Y (2000) Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol 124:949–958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Behera UK, Rautaray SK (2010) Effects of biofertilizers on productivity and quality parameters of durum wheat (Triticum turgidum) on a vertisol of Central India. Arch Agron Soil Sci 56:65–72

    Article  CAS  Google Scholar 

  • Berta G, Fusconi A, Trotta A, Scannerini S (1990) Morphogenetic modifications induced by the mycorrhizal fungus Glomus strain E3 in the root system of Allium porrum L. New Phytol 114:207–215

    Article  Google Scholar 

  • Blanke V, Wagner M, Renker C, Lippert H, Michulitz M, Kuhn AJ, Buscot F (2011) Arbuscular mycorrhizas in phosphate-polluted soil: interrelations between root colonization and nitrogen. Plant Soil 343:379–392

    Article  CAS  Google Scholar 

  • Blum A (1998) Improving wheat grain filling under stress by stem reserve mobilisation. Euphytica 100:77–83

    Article  Google Scholar 

  • Börstler B, Raab PA, Thiéry O, Morton JB, Redecker D (2008) Genetic diversity of the arbuscular mycorrhizal fungus Glomus intraradices as determined by mitochondrial large subunit rRNA gene sequences is considerably higher than previously expected. New Phytol 180:452–465

    Article  PubMed  Google Scholar 

  • Cabral C, Ravnskov S, Tringovska I, Wollenweber B (2016) Arbuscular mycorrhizal fungi modify nutrient allocation and composition in wheat (Triticum aestivum L.) subjected to heat-stress. Plant Soil 408:385–399

    Article  CAS  Google Scholar 

  • Cavagnaro TR (2008) The role of arbuscular mycorrhizas in improving plant zinc nutrition under low soil zinc concentrations: a review. Plant Soil 304:315–325

    Article  CAS  Google Scholar 

  • Ciccolini V, Bonari E, Pellegrino E (2015) Land-use intensity and soil properties shape the composition of fungal communities in Mediterranean peaty soils drained for agricultural purposes. Biol Fertil Soils 51:719–731

    Article  Google Scholar 

  • Clarke KR, Gorley RN (2006) Primer Primer-E, Plymouth

  • D’Amato F (1989) The progress of Italian wheat production in the first half of the 20th century: the contribution of breeders. Agr Med 119:157–174

    Google Scholar 

  • Daniell TJ, Husband R, Fitter AH, Young JPW (2001) Molecular diversity of arbuscular mycorrhizal fungi colonising arable crops. FEMS Microbiol Ecol 36:203–209

    Article  CAS  PubMed  Google Scholar 

  • De Vita P, Maggio A (2006) Yield stability analysis in durum wheat: progress over the last two decades in Italy. Cereal Res Commun 34:1207–1214

    Article  Google Scholar 

  • De Vita P, Nicosia OLD, Nigro F, Platani C, Riefolo C, Di Fonzo N, Cattivelli L (2007) Breeding progress in morpho-physiological, agronomical and qualitative traits of durum wheat cultivars released in Italy during the 20th century. Eur J Agron 26:39–53

    Article  Google Scholar 

  • Dinelli G, Carretero AS, Di Silvestro R, Marotti I, Fu S, Benedettelli S, Ghiselli L, Gutiérrez AF (2009) Determination of phenolic compounds in modern and old varieties of durum wheat using liquid chromatography coupled with time-of-flight mass spectrometry. J Chromatogr A 1216:7229–7240

    Article  CAS  PubMed  Google Scholar 

  • Dinelli G, Segura-Carretero A, Di Silvestro R, Marotti I, Arráez-Román D, Benedettelli S, Ghiselli L, Fernadez-Gutierrez A (2011) Profiles of phenolic compounds in modern and old common wheat varieties determined by liquid chromatography coupled with time-of-flight mass spectrometry. J Chromatogr A 1218:7670–7681

    Article  CAS  PubMed  Google Scholar 

  • Dinelli G, Marotti I, Di Silvestro R, Bosi S, Bregola V, Accorsi M, Di Loreto A, Benedettelli S, Ghiselli L, Catizone P (2013) Agronomic, nutritional and nutraceutical aspects of durum wheat (Triticum durum Desf.) cultivars under low input agricultural management. Ital J Agron 8:85–93

    Google Scholar 

  • Duan J, Tian H, Drijber RA, Gao Y (2015) Systemic and local regulation of phosphate and nitrogen transporter genes by arbuscular mycorrhizal fungi in roots of winter wheat (Triticum aestivum L.) Plant Physiol Biochem 96:199–208

    Article  CAS  PubMed  Google Scholar 

  • Ellouze W, Hamel C, DePauw RM, Knox RE, Cuthbert RD, Singh AK (2015) Potential to breed for mycorrhizal association in durum wheat. Can J Microbiol 62:263–271

    Article  PubMed  Google Scholar 

  • Ercoli L, Lulli L, Arduini I, Mariotti M, Masoni A (2011) Durum wheat grain yield and quality as affected by S rate under Mediterranean conditions. Eur J Agron 35:63–70

    Article  CAS  Google Scholar 

  • Ercoli L, Arduini I, Mariotti M, Lulli L, Masoni A (2012) Management of sulphur fertiliser to improve durum wheat production and minimise S leaching. Eur J Agron 38:74–82

    Article  CAS  Google Scholar 

  • Ercoli L, Masoni A, Pampana S, Mariotti M, Arduini I (2013) As durum wheat productivity is affected by nitrogen fertilisation management in Central Italy. Eur J Agron 44:38–45

    Article  CAS  Google Scholar 

  • Ferrante A, Savin R, Slafer GA (2012) Floret development and grain setting differences between modern durum wheats under contrasting nitrogen availability. J Exp Bot 64:169–184

    Article  PubMed  PubMed Central  Google Scholar 

  • Fitter AH, Helgason T, Hodge A (2011) Nutritional exchanges in the arbuscular mycorrhizal symbiosis: implications for sustainable agriculture. Fungal Genet Biol 25:68–72

    Article  Google Scholar 

  • Gao X, Akhter F, Tenuta M, Flaten DN, Gawalko EJ, Grantc CA (2010) Mycorrhizal colonization and grain cd concentration of field-grown durum wheat in response to tillage, preceding crop and phosphorus fertilization. J Sci Food Agric 90:750–758

    CAS  PubMed  Google Scholar 

  • Gebbing T, Schnyder H (1999) Pre-anthesis reserve utilization for protein and carbohydrate synthesis in grains of wheat. Plant Physiol 121:871–878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giagnoni L, Pastorelli R, Mocali S, Arenella M, Nannipieri P, Renella G (2016) Availability of different nitrogen forms changes the microbial communities and enzyme activities in the rhizosphere of maize lines with different nitrogen use efficiency. Appl Soil Ecol 98:30–38

    Article  Google Scholar 

  • Gianinazzi S, Gollotte A, Binet MN, van Tuinen D, Redecker D, Wipf D (2010) Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20:519–530

    Article  PubMed  Google Scholar 

  • He X, Nara K (2007) Element biofortification: can mycorrhizas potentially offer a more effective and sustainable pathway to curb human malnutrition? Evolution 57:2742–2752

    Google Scholar 

  • Helgason T, Daniell TJ, Husband R, Fitter AH, Young JPW (1998) Ploughing up the wood-wide web? Nature 394:431–431

    Article  CAS  PubMed  Google Scholar 

  • Hetrick BD, Bloom J (1984) The influence of temperature on colonization of winter wheat by vesicular-arbuscular mycorrhizal fungi. Mycologia 76:953–956

    Article  Google Scholar 

  • Hetrick BAD, Wilson GWT, Cox TS (1992) Mycorrhizal dependence of modern wheat varieties, landraces, and ancestors. Can J Bot 70:2032–2040

    Article  Google Scholar 

  • Hetrick BAD, Wilson GWT, Cox TS (1993) Mycorrhizal dependence of modern wheat cultivars and ancestors: a synthesis. Can J Bot 71:512–518

    Article  Google Scholar 

  • Hijri I, Sýkorová Z, Oehl F, Ineichen K, Mäder P, Wiemken A, Redecker D (2006) Communities of arbuscular mycorrhizal fungi in arable soils are not necessarily low in diversity. Mol Ecol 15:2277–2289

    Article  CAS  PubMed  Google Scholar 

  • Hildermann I, Messmer M, Dubois D, Boller T, Wiemken A, Mäder P (2010) Nutrient use efficiency and arbuscular mycorrhizal root colonization of winter wheat cultivars in different farming systems of the DOK long-term trial. J Sci Food Agric 90:2027–2038

    CAS  PubMed  Google Scholar 

  • Hodge A, Storer K (2015) Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems. Plant Soil 386:1–19

    Article  CAS  Google Scholar 

  • Hodge A, Berta G, Doussan C, Merchan F, Crespi M (2009) Plant root growth, architecture and function. Plant Soil 32:153–187

    Article  Google Scholar 

  • Isaac RA, Johnson WC, Kalra Y (1998) Elemental determination by inductively coupled plasma atomic emission spectrometry. In: Handbook and reference methods for plant analysis. CRC Press, New York, pp 165–170

    Google Scholar 

  • IUSS Working Group WRB World reference base for soil resources (2006).World Soil Resources Reports No. 103. FAO, Rome.

  • Jones JB Jr, Wolf B, Mills HA (1991) Plant Analysis Handbook II: a practical sampling, preparation, analysis, and interpretation guide. Micro-Macro Publishing Inc., Athens

    Google Scholar 

  • Kohout P, Sudová R, Janoušková M, Čtvrtlíková M, Hejda M, Pánková H, Slavíková R, Štajerová K, Vosátka M, Sýkorová Z (2014) Comparison of commonly used primer sets for evaluating arbuscular mycorrhizal fungal communities: Is there a universal solution?. Soil Biol Biochem 68:482–493

  • Kottek M, Grieser J, Beck C, Rudolf B, Rubel F (2006) World map of the Köppen-Geiger climate classification updated. Meteorol Z 15:259–263

    Article  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

  • Krüger M, Krüger C, Walker C, Stockinger H, Schüßler A (2012) Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level. New Phytol 193:970–984

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  Google Scholar 

  • Lee J, Lee S, Young JPW (2008) Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 65:339–349

    Article  CAS  PubMed  Google Scholar 

  • Lehmann A, Rillig MC (2015) Arbuscular mycorrhizal contribution to copper, manganese and iron nutrient concentrations in crops - a meta-analysis. Soil Biol Biochem 81:147–158

    Article  CAS  Google Scholar 

  • Lehmann A, Veresoglou SD, Leifheit EF, Rillig MC (2014) Arbuscularmycorrhizal influence on zinc nutrition in crop plants - a meta-analysis. Soil Biol Biochem 69:123-131Li H, Smith SE, Holloway RE, Zhu Y, Smith FA (2006) Arbuscular mycorrhizal fungi contribute to phosphorus uptake by wheat grown in a phosphorus-fixing soil even in the absence of positive growth responses. New Phytol 172:536–543

    Google Scholar 

  • Li H, Smith SE, Holloway RE, Zhu Y, Smith FA (2006) Arbuscular mycorrhizal fungi contribute to phosphorus uptake by wheat grown in a phosphorus-fixing soil even in the absence of positive growth responses. New Phytol 172:536-543

  • Lindsay WL, Norvell WA (1978) Development of a DTPA soil test for zinc, iron, manganese, and copper. Soil Sci Soc Am J 42:421–428

    Article  CAS  Google Scholar 

  • McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular–arbuscular mycorrhizal fungi. New Phytol 115:495–501

    Article  Google Scholar 

  • Mohammad MJ, Pan WL, Kennedy AC (1998) Seasonal mycorrhizal colonization of winter wheat and its effect on wheat growth under dryland field conditions. Mycorrhiza 8:139–144

    Article  Google Scholar 

  • Mohammad A, Mitra B, Khan AG (2004) Effects of sheared-root inoculum of Glomus intraradices on wheat grown at different phosphorus levels in the field. Agric Ecosyst Environ 103:245–249

    Article  Google Scholar 

  • Mosse B (1986) Mycorrhiza in a sustainable agriculture. Biol Agric Hortic 3:191–209

    Article  Google Scholar 

  • Mueller ND, Gerber JS, Johnston M, Ray DK, Ramankutty N, Foley JA (2012) Closing yield gaps through nutrient and water management. Nature 490:254–257

    Article  CAS  PubMed  Google Scholar 

  • Myers SS, Zanobetti A, Kloog I, Huybers P, Leakey AD, Bloom AJ, Carlisle E, Dietterich LH, Fitzgerald G, Hasegawa T, Holbrook NM, Nelson RL, Ottman ML, Raboy V, Sakai H, Sartor KA, Schwartz J, Seneweera S, Tausz M, Usui Y (2014) Increasing CO2 threatens human nutrition. Nature 510:139–142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Newsham KK, Fitter AH, Watkinson AR (1995) Multi-functionality and biodiversity in arbuscular mycorrhizas. Trends Ecol Evol 10:407–411

    Article  CAS  PubMed  Google Scholar 

  • Oliveira HR, Campana MG, Jones H, Hunt HV, Leigh F, Redhouse DI, Lister DL, Jones MK (2012) Tetraploid wheat landraces in the Mediterranean basin: taxonomy, evolution and genetic diversity. PLoS One 7:e37063

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oliveira RS, Rocha I, Ma Y, Vosátka M, Freitas H (2016) Seed coating with arbuscular mycorrhizal fungi as an ecotechnologicalapproach for sustainable agricultural production of common wheat (Triticum aestivum L.) Jpn J Tox Env Health 79:329–337

    Article  CAS  Google Scholar 

  • Palta JA, Kobata T, Turner NC, Fillery IR (1994) Remobilization of carbon and nitrogen in wheat as influenced by postanthesis water deficits. Crop Sci 34:118–124

    Article  Google Scholar 

  • Pellegrino E, Turrini A, Gamper HA, Cafà G, Bonari E, Young JPW, Giovannetti M (2012) Establishment: persistence and effectiveness of arbuscular mycorrhizal fungal inoculants in the field revealed using molecular genetic tracing and measurement of yield components. New Phytol 194:810–822

    Article  CAS  PubMed  Google Scholar 

  • Pellegrino E, Bosco S, Ciccolini V, Pistocchi C, Sabbatini T, Silvestri N, Bonari E (2015a) Agricultural abandonment in Mediterranean reclaimed peaty soils: long-term effects on soil chemical properties, arbuscular mycorrhizas and CO2 flux. Agric Ecosyst Environ 199:164–175

    Article  CAS  Google Scholar 

  • Pellegrino E, Öpik M, Bonari E, Ercoli L (2015b) Responses of wheat to arbuscular mycorrhizal fungi: A meta-analysis of field studies from 1975 to 2013. Soil Biol Biochem 84:210–217

    Article  CAS  Google Scholar 

  • Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. T Brit Mycol Soc 55:158–161

    Article  Google Scholar 

  • Rascio A, Picchi V, Naldi JP, Colecchia S, De Santis G, Gallo A, Carlino E, Lo Scalzo R, De Gara L (2015) Effects of temperature increase, through spring sowing, on antioxidant power and health-beneficial substances of old and new wheat varieties. J Cereal Sci 61:111–118

    Article  CAS  Google Scholar 

  • Redecker D (2000) Specific PCR primers to identify arbuscular mycorrhizal fungi within colonized roots. Mycorrhiza 10:73–80

    Article  CAS  Google Scholar 

  • Redecker D, Hijri I, Wiemken A (2003) Molecular identification of arbuscular mycorrhizal fungi in roots: perspectives and problems. Folia Geobot 38:113–124

    Article  Google Scholar 

  • Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 171:41–53

    Article  CAS  PubMed  Google Scholar 

  • Royo C, Álvaro F, Martos V, Ramdani A, Isidro J, Villegas D, Del Moral LFG (2007) Genetic changes in durum wheat yield components and associated traits in Italian and Spanish varieties during the twentieth century. Euphytica 155:259–270

    Article  Google Scholar 

  • Rozbicki J, Ceglińska A, Gozdowski D, Jakubczak M, Cacak-Pietrzak G, Mądry W, Golba J, Piechociński M, Sobczyński G, Studnicki M, Drzazga T (2015) Influence of the cultivar, environment and management on the grain yield and bread-making quality in winter wheat. J Cereal Sci 61:126–132

    Article  Google Scholar 

  • Saia S, Rappa V, Ruisi P, Abenavoli MR, Sunseri F, Giambalvo D, Frenda AS, Martinelli F (2015a) Soil inoculation with symbiotic microorganisms promotes plant growth and nutrient transporter genes expression in durum wheat. Front Plant Sci 6:1–10

    Article  Google Scholar 

  • Saia S, Ruisi P, Fileccia V, Di Miceli G, Amato G, Martinelli F (2015b) Metabolomics suggests that soil inoculation with arbuscular mycorrhizal fungi decreased free amino acid content in roots of durum wheat grown under N-limited, P-rich field conditions. PLoS One 10:e0129591

    Article  PubMed  PubMed Central  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Schüßler A, Walker C (2010) The Glomeromycota: a species list with new families and new genera. Edinburgh & Kew: The Royal Botanic Garden; Munich, Germany: Botanische Staatssammlung Munich: Oregon State University. URL: http://www.amf-phylogeny.com. ISBN-13: 978–1,466,388,048; ISBN-10:1,466,388,048.

  • Siddique KHM, Tennant D, Perry MW, Belford RK (1990) Water use and water use efficiency of old and modern wheat cultivars in a Mediterranean-type environment. Crop Pasture Sci 41:431–447

    Article  Google Scholar 

  • Singh AK, Hamel C, DePauw RM, Knox RE (2012) Genetic variability in arbuscular mycorrhizal fungi compatibility supports the selection of durum wheat genotypes for enhancing soil ecological services and cropping systems in Canada. Can J Microbiol 58:293–302

    Article  CAS  PubMed  Google Scholar 

  • Slafer GA, Savin R, Sadras VO (2014) Coarse and fine regulation of wheat yield components in response to genotype and environment. Field Crop Res 157:71–83

    Article  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic Press, Amsterdam

    Google Scholar 

  • Smith SE, Jakobsen I, Grønlund M, Smith FA (2011) Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol 156:1050–1057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soil Survey Staff (1975) Soil taxonomy: a basic system of soil classification for making and interpreting soil surveys. USDA-SCS Agric. Handb. 436. U.S. Gov. Print. Office, Washington, DC

    Google Scholar 

  • Stagnari F, Onofri A, Codianni P, Pisante M (2013) Durum wheat varieties in N-deficient environments and organic farming: a comparison of yield, quality and stability performances. Plant Breed 132:266–275

    Article  CAS  Google Scholar 

  • Stockinger H, Walker C, Schüßler A (2009) ‘Glomus intraradices DAOM197198’, a model fungus in arbuscular mycorrhiza research, is not Glomus intraradices. New Phytol 183:1176–1187

    Article  PubMed  Google Scholar 

  • Stöppler H, Kölsch E, Vogtmann H (1990) Vesicular-arbuscular mycorrhiza in varieties of winter wheat in a low external input system. Biol Agric Hortic 7:191–199

    Article  Google Scholar 

  • Suri VK, Choudhary AK, Chander G, Verma TS (2011) Influence of vesicular arbuscular-mycorrhizal fungi and applied phosphorus on root colonization in wheat and plant nutrient dynamics in a phosphorus-deficient acid alfisol of western Himalayas. Commun Soil Sci Plan 42:1177–1186

    Article  CAS  Google Scholar 

  • Sýkorová Z, Börstler B, Zvolenská S, Fehrer J, Gryndler M, Vosátka M, Redecker D (2012) Long-term tracing of Rhizophagus irregularis isolate BEG140 inoculated on Phalaris arundinacea in a coal mine spoil bank, using mitochondrial large subunit rDNA markers. Mycorrhiza 22:69–80

    Article  PubMed  Google Scholar 

  • Thiéry O, Börstler B, Ineichen K, Redecker D (2010) Evolutionary dynamics of introns and homing endonuclease ORFs in a region of the large subunit of the mitochondrial rRNA in Glomus species (arbuscular mycorrhizal fungi, Glomeromycota). Mol Phylogenet Evol 55:599–610

    Article  PubMed  Google Scholar 

  • Tilman D, Balzer C, Hill J, Befort BL (2011) Global food demand and the sustainable intensification of agriculture. P Natl Acad Sci USA 108:20260–20264

    Article  CAS  Google Scholar 

  • Uauy C, Distelfeld A, Fahima T, Blechl A, Dubcovsky J (2006) A NAC gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science 314:1298–1301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vallebona C, Pellegrino E, Frumento P, Bonari E (2015) Temporal trends in extreme rainfall intensity and erosivity in the Mediterranean region: a case study in southern Tuscany, Italy. Clim Chang 128:139–151

    Article  Google Scholar 

  • Van Diepen LT, Lilleskov EA, Pregitzer KS, Miller RM (2007) Decline of arbuscular mycorrhizal fungi in northern hardwood forests exposed to chronic nitrogen additions. New Phytol 176:175–183

    Article  PubMed  Google Scholar 

  • White PJ, Broadley MR (2009) Biofortification of crops with seven mineral elements often lacking in human diets - iron, zinc, copper, calcium, magnesium, selenium and iodine. New Phytol 182:49–84

    Article  CAS  PubMed  Google Scholar 

  • Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Res 14:415–421

    Article  Google Scholar 

  • Zhang W, Liu D, Liu Y, Cui Z, Chen X, Zou C (2016) Zinc uptake and accumulation in winter wheat relative to changes in root morphology and mycorrhizal colonization following varying phosphorus application on calcareous soil. Field Crop Res 197:74–82

    Article  Google Scholar 

  • Zhu YG, Smith SE, Barritt AR, Smith FA (2001) Phosphorus (P) efficiencies and mycorrhizal responsiveness of old and modern wheat cultivars. Plant Soil 237:249–255

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Institute of Life Sciences, Scuola Superiore Sant’Anna, Piazza Martiri della Libertà 33, 56127, Pisa, Italy

    Laura Ercoli & Elisa Pellegrino

  2. Symplanta GmbH & Co. KG, Milanweg 46, 26127, Oldenburg, Germany

    Arthur Schüßler

  3. Department of Agriculture, Food and Environment, University of Pisa, via del Borghetto 80, 56124, Pisa, Italy

    Iduna Arduini

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  1. Laura Ercoli
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  4. Elisa Pellegrino
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Correspondence to Laura Ercoli.

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Ercoli, L., Schüßler, A., Arduini, I. et al. Strong increase of durum wheat iron and zinc content by field-inoculation with arbuscular mycorrhizal fungi at different soil nitrogen availabilities. Plant Soil 419, 153–167 (2017). https://doi.org/10.1007/s11104-017-3319-5

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